The Use of Natural Genetic Diversity in the Understanding of Metabolic Organization and Regulation

The study of metabolic regulation has traditionally focused on analysis of specific enzymes, emphasizing kinetic properties, and the influence of protein interactions and post-translational modifications. More recently, reverse genetic approaches permit researchers to directly determine the effects of a deficiency or a surplus of a given enzyme on the biochemistry and physiology of a plant. Furthermore, in many model species, gene expression atlases that give important spatial information concerning the quantitative expression level of metabolism-associated genes are being produced. In parallel, “top-down” approaches to understand metabolic regulation have recently been instigated whereby broad genetic diversity is screened for metabolic traits and the genetic basis of this diversity is defined thereafter. In this article we will review recent examples of this latter approach both in the model species Arabidopsis thaliana and the crop species tomato (Solanum lycopersicum). In addition to highlighting examples in which this genetic diversity approach has proven promising, we will discuss the challenges associated with this approach and provide a perspective for its future utility

Meta-analysis of genome-wide association studies provides insights into genetic control of tomato flavor

Tomato flavor has changed over the course of long-term domestication and intensive breeding. To understand the genetic control of flavor, we report the meta-analysis of genome-wide association studies (GWAS) using 775 tomato accessions and 2,316,117 SNPs from three GWAS panels. We discover 305 significant associations for the contents of sugars, acids, amino acids, and flavor-related volatiles. We demonstrate that fruit citrate and malate contents have been impacted by selection during domestication and improvement, while sugar content has undergone less stringent selection. We suggest that it may be possible to significantly increase volatiles that positively contribute to consumer preferences while reducing unpleasant volatiles, by selection of the relevant allele combinations. Our results provide genetic insights into the influence of human selection on tomato flavor and demonstrate the benefits obtained from meta-analysis.J-T.Z. was funded by a Chinese Scholarship Council (CSC) scholarship

Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition

The unique flavour of a tomato fruit is the sum of a complex interaction among sugars, acids, and a large set of volatile compounds. While it is generally acknowledged that the flavour of commercially produced tomatoes is inferior, the biochemical and genetic complexity of the trait has made breeding for improved flavour extremely difficult. The volatiles, in particular, present a major challenge for flavour improvement, being generated from a diverse set of lipid, amino acid, and carotenoid precursors. Very few genes controlling their biosynthesis have been identified. New quantitative trait loci (QTLs) that affect the volatile emissions of red-ripe fruits are described here. A population of introgression lines derived from a cross between the cultivated tomato Solanum lycopersicum and its wild relative, S. habrochaites, was characterized over multiple seasons and locations. A total of 30 QTLs affecting the emission of one or more volatiles were mapped. The data from this mapping project, combined with previously collected data on an IL population derived from a cross between S. lycopersicum and S. pennellii populations, were used to construct a correlational database. A metabolite tree derived from these data provides new insights into the pathways for the synthesis of several of these volatiles. One QTL is a novel locus affecting fruit carotenoid content on chromosome 2. Volatile emissions from this and other lines indicate that the linear and cyclic apocarotenoid volatiles are probably derived from separate carotenoid pools

Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family

Arabidopsis thaliana has nine genes that constitute a family of putative carotenoid cleavage dioxygenases (CCDs). While five members of the family are believed to be involved in synthesis of the phytohormone abscisic acid, the functions of the other four enzymes are less clear. Recently two of the enzymes, CCD7/MAX3 and CCD8/MAX4, have been implicated in synthesis of a novel apocarotenoid hormone that controls lateral shoot growth. Here, we report on the molecular and genetic interactions between CCD1, CCD7/MAX3 and CCD8/ MAX4. CCD1 distinguishes itself from other reported CCDs as being the only member not targeted to the plastid. Unlike ccd7/max3 and ccd8/max4, both characterized as having highly branched phenotypes, ccd1 loss-of-function mutants are indistinguishable from wild-type plants. Thus, even though CCD1 has similar enzymatic activity to CCD7/MAX3, it does not have a role in synthesis of the lateral shoot growth inhibitor. Rather, it may have a role in synthesis of apocarotenoid flavor and aroma volatiles, especially in maturing seeds where loss of function leads to significantly higher carotenoid levels